2719
The Journal of Experimental Biology 202, 2719–2726 (1999)
Printed in Great Britain © The Company of Biologists Limited 1999
JEB2151
THE DEVELOPMENT OF A BIOLOGICAL NOVELTY: A DIFFERENT WAY TO MAKE
APPENDAGES AS REVEALED IN THE SNOUT OF THE STAR-NOSED MOLE
CONDYLURA CRISTATA
KENNETH C. CATANIA1,*, R. GLENN NORTHCUTT2 AND JON H. KAAS1
1Department of Psychology, Vanderbilt University, 301 Wilson Hall, Nashville, TN 37240, USA and 2Department of
Neurosciences, 0201, University of California, San Diego, 9500 Gilman Drive, La Jolla, CA 92093-0201, USA
*e-mail: Catania@ctrvax.vanderbilt.edu
Accepted 8 July; published on WWW 30 September 1999
Summary
The nose of the star-nosed mole Condylura cristata is a
only at the tip of the snout. As a result of this unique
‘unfolding’ formation, the rostral end of each adult
complex biological novelty consisting of 22 epidermal
appendage is derived from caudal embryonic facial tissue,
appendages. How did this new set of facial appendages
while the caudal end of each appendage is derived from
arise? Recent studies find remarkable conservation of the
rostral facial tissue. This developmental process has
genes expressed during appendage formation across phyla,
essentially no outgrowth phase and results in the reversal
suggesting that the basic mechanisms for appendage
development are ancient. In the nose of these moles,
of the original embryonic orientation of each appendage.
however, we find a unique pattern of appendage
This differs from the development of other known
appendages, which originate either as outgrowths of the
morphogenesis, showing that evolution is capable of
body wall or from subdivisions of outgrowths (e.g. tetrapod
constructing appendages in different ways. During
digits). Adults of a different mole species (Scapanus
development, the nasal appendages of the mole begin as a
townsendii) exhibit a star-like pattern that resembles an
series of waves in the epidermis. A second deep layer of
embryonic stage of the star-nosed mole, suggesting that the
epidermis then grows under these superficial epidermal
development of the star recapitulates stages of its evolution.
waves to produce 22 separate, elongated epidermal
cylinders embedded in the side of the mole’s face. The
caudal end of each cylinder later erupts from the face and
Key words: ontogeny, phylogeny, evolution, recapitulation,
homology, star-nosed mole, Condylura cristata.
rotates forward to project rostrally, remaining attached
Introduction
Animal appendages come in a variety of forms, such as the
legs, wings and antennae of arthropods, the fins of fish, the
limbs and digits of mammals and the defensive spines of sea
urchins, to name a few. Despite a wide variety in structure and
function, all these appendages originate in the same basic way,
as outgrowths of the body wall (for reviews, see Panganiban
et al., 1997; Shubin et al., 1997) or as subdivisions of
outgrowths in the case of tetrapod digits (Hamburger and
Hamilton, 1951; Hinchliffe and Johnson, 1980). Perhaps this
is not too surprising, since recent studies reveal a remarkable
conservation of the regulatory genes and signaling molecules
that underlie early appendage development (Averof and
Cohen, 1997; Basler and Struhl, 1994; Ferrari et al., 1995;
Panganiban et al., 1994, 1995, 1997; Popadic et al., 1998;
Shubin et al., 1997). The conservation of these regulatory
elements across metazoan phyla suggests that new appendages
may have arisen primarily from the redeployment of ancient
developmental mechanisms (Panganiban et al., 1997; Raff,
1996; but see also Gerhart and Kirschner, 1997a; Williams,
1998). This raises basic questions about the process and course
of evolution. Does the invention of new methods of appendage
morphogenesis represent a major hurdle to the process of
evolution? Or has it simply been most efficient to re-use and
modify existing developmental pathways?
One way to address these questions is to examine the
development of novel and recently evolved animal appendages
to see whether they make use of conserved mechanisms of
morphogenesis. The star-nosed mole (Condylura cristata)
possesses just such a set of appendages in a ring around its
snout. The star-nosed mole is a eutherian mammal thought to
have diverged from other moles in the last 30 million years
(Moore, 1986; Skoczen, 1993). Its nose is surrounded by 22
fleshy and mobile appendages that are not homologous to
body-wall extensions in other species. They are unique not
only in their location and appearance, but also in their function.
They form a touch organ of unparalleled complexity and acuity
(Catania, 1995a, 1996). The star functions much like a tactile
eye, with a small but high-resolution pair of central appendages
2720 K. C. CATANIA, R. G. NORTHCUTT AND J. H. KAAS
and a number of larger, low-resolution peripheral appendages
(Catania and Kaas, 1995, 1997).
One might ask whether these nasal structures are comparable
as ‘appendages’ to the body-wall extensions of other
metazoans. Though of relatively recent origin, an examination
of their anatomy reveals them to be elaborate structures that
integrate a number of tissue systems for their sensory functions
(Catania, 1995a, 1996). The outer surface of each appendage
is an epidermal layer covered with complex tactile sensory
organs termed Eimer’s organs. Each appendage is densely
innervated by a separate branch of the infraorbital nerve, which
runs through its center. The appendages are moved by a series
of tendons that attach to muscles on the side of the face, and
each appendage has its own blood supply (Grand et al., 1998).
In addition, the touch centers of the central nervous system of
the star-nosed mole are subdivided to represent sensory
information from each appendage in a separate module
(Catania and Kaas, 1995, 1996). Thus, these appendages are
clearly on a par with other animal appendages in complexity,
and their evolution has involved the integrated manipulation of
multiple tissue systems, including the dermis, epidermis,
tendons, muscles and peripheral nervous and circulatory
systems.
Were established mechanisms of appendage morphogenesis
co-opted to produce this recently evolved set of appendages?
We examined the development of the nasal appendages in
embryonic and juvenile moles and found that they form in a
manner unlike any developmental sequence previously
described.
Materials and methods
To examine the development of the nasal appendages that
form the star, we collected a developmental series of embryos
from wild-caught star-nosed moles (Condylura cristata Illiger
1811). For post-natal stages, captured pregnant moles were
housed in our laboratory where (for the first time) they gave
birth and raised litters of young in captivity. Star-nosed moles
are seasonal breeders and give birth to a single litter of young
in the spring (Eadie and Hamilton, 1956). We were able to
collect pregnant females during March and April using
Sherman traps under Pennsylvania scientific collecting permit
number COL00087. The day of fertilization is unknown
because mating took place in the wild, and all embryos were
therefore staged by crown–rump length. Moles were killed
with Nembutal (110 mg kg−1), and embryos were fixed in a
mixture of 1 % paraformaldehyde and 2 % glutaraldehyde in
phosphate buffer (for scanning electron microscopy or serial
sections) or in 4 % paraformaldehyde in phosphate buffer (for
neuronal tract tracing). Postnatal development was examined
in newborn moles from females that gave birth and raised
young in the laboratory. Pregnant females were kept in moist
peat moss, given free access to water and fed night-crawlers
(Lumbricus terrestris) ad libitum. Juvenile moles were killed
and fixed as above.
Tissue from each stage was examined under the scanning
electron microscope and serial thin-sectioned for light
microscopy. In addition, innervation patterns were determined
using the lipophilic neuronal tracer 1,1′-dioctadecyl-3,3,3′,3′tetramethylindocarbocyanine perchlorate (DiI) (Molecular
Probes Inc.) and a scanning confocal microscope. For scanning
electron microscopy, specimens were dehydrated through an
ethanol series to 100 % ethanol, and then transferred into a
critical-point dryer where the alcohol was replaced with liquid
carbon dioxide. After drying, specimens were sputter-coated
with gold and viewed in a Cambridge 360 Stereoscan scanning
electron microscope.
To examine the histology of the nose, tissue was post-fixed
in 1 % osmium tetroxide, dehydrated in a graded ethanol series
and transferred into propylene oxide. Tissue was embedded
in Embed 812 epoxy resin (EM Sciences). Semi-thin
serial sections (1–2 µm) were cut transversely on an LKB
ultramicrotome and stained with 1 % Toluidine Blue. To
determine innervation patterns, the tip of the snout was
removed from selected paraformaldehyde-fixed specimens,
and DiI crystals were applied to exposed nerve fascicles. After
4 weeks of transport at room temperature, the tissue was
examined under the scanning confocal microscope. All
procedures were approved by the Vanderbilt University
Animal Care and Use Committee and are in compliance with
NIH guidelines for the care and use of laboratory animals.
Results
In this study, the development of the nasal appendages is
examined for a series of five prenatal (Figs 1–3) and three
postnatal stages (Fig. 4). The star is formed by 11 symmetrical
pairs of appendages surrounding the nostrils. The appendages
are numbered from 1 to 11 on each side of the face, beginning
with the dorsal-most appendage. Figs 2 and 3 show DiI-filled
and labeled nerve fibers for selected specimens, illustrating
important stages in the development of innervation patterns.
The earliest stage described is the 9 mm crown–rump length
embryo (Fig. 1A). At this stage, there is no sign of the nasal
appendages that will eventually form the star. The tip of the
nose appears smooth and uniform in the scanning electron
microscope. Transverse sections through the nasal epidermis
(nose sections, Fig. 1A) also reveal a smooth thin epidermis
approximately 40 µm in thickness surrounding the underlying
dermis and mesenchyme. At this early stage, the epidermis is
contacted by many fascicles of nerve fibers that form a dense
subcutaneous network (Fig. 2A). At high magnification (not
shown), growth cones are visible at the distal ends of the nerve
fascicles. But there is no indication, however, from either the
epidermal tissue or the innervation patterns of how or where
the appendages of the star will later form.
The first signs of the nasal appendages are seen in 11 mm
embryos (Fig. 1B). A series of rostro–caudally oriented
swellings appears along the side of the face. Each swelling is
the precursor to a single nasal appendage, and each consists of
simply a ‘buckling’ or slight wave in the epidermis. The
swellings form first along the midline, and later laterally so that
Development of the mole’s star nose 2721
Fig. 1. The embryonic development of the star. (A–E) A series of
successive stages in the prenatal development of the star-nosed mole.
(A) In 9 mm embryos, the nose is undifferentiated and consists of a
smooth thin epidermis. (B) In 11 mm embryos, the primordial
appendages first appear as a series of epidermal swellings. Nose
sections show that these swellings consist of simple ‘waves’ in the thin
epidermis (numbered 1–5). (C) In 13 mm embryos, all 11 primordial
appendages are present as pronounced raised areas of the epidermis.
Although the star appears superficially well formed, the appendages are
still simple waves in the epidermis with no separation from the lumen
of the central snout. (D) In 15 mm embryos, the bottom wall of each
appendage forms as a new deep layer of epidermis (arrow) extends to separate each epidermal wave from the dermis and mesenchyme of the
snout. (E) Just before birth, in 20 mm embryos, there is a proliferation of cells in the epidermis of the snout, and each separate appendage forms
a cylinder embedded in the hypertrophied epidermis (arrowheads). At the same time, the external pattern of appendages on the snout is
obscured. Scale bar, 250 µm.
the precursors to appendages 1–5 and 10 and 11 appear before
the swellings for the lateral appendages. Transverse sections
through the snout reveal the epidermal waves that make up the
appendages (Fig. 1B). At these early stages, the myelin-poor
nerve fascicles are not apparent in light microscopy, but DiI
labeling reveals a very dense innervation of the epidermis. The
crest of each epidermal wave is contacted by numerous nerve
fascicles that project from the center of the snout (Fig. 2B).
The simple conformational change of the epidermis into crests
and troughs seems to be the first foundation for the selective
elimination or preservation of innervating nerve fibers. Where
the waves have formed, nerve fibers densely contact the crests
of the waves and are sparse in the troughs (Fig. 3A1), but in
the lateral areas where the waves have not yet formed, there is
a uniform distribution of nerve fibers (Fig. 3A2).
In 13 mm and 15 mm embryos, all 22 appendages of the star
are clearly apparent (Fig. 1C,D). Here, the star appears
remarkably adult-like, as if the appendages were folded against
the side of the face, but this external appearance is an illusion.
In 13 mm embryos, the appendages are still simple waves or
swellings of the epidermis (see nose section, Fig. 1C) and are
open to the mesenchyme of the central snout. The epidermis
of the waves has become more densely innervated from ingrowing fibers, and the nerve fascicles are well segregated to
individual crests in the epidermis (Figs 2C, 3B). At high
magnification, there is not yet any sign of the orderly
arrangements of nerve fibers that characterize the punctate
epidermal sensory organs in the adult skin (Catania, 1995a).
Instead, the nerve fascicles end in amorphous collections of
terminals extending numerous filopodia and often distinct
growth cones (arrowhead, Fig. 3B2).
During these stages (13–15 mm crown–rump), a complex
sequence of tissue growth and movement takes place,
separating each of the epidermal waves into a distinct unit with
a lumen and surrounding walls. A new deep layer of epidermis
begins to grow beneath the innervated epidermal waves. This
2722 K. C. CATANIA, R. G. NORTHCUTT AND J. H. KAAS
Fig. 2. The innervation of the nose at selected developmental stages, revealed by the lipophilic neuronal tracer DiI. (A) In 9mm embryos, there is
a uniform innervation of the epidermal walls that form the snout, but no pattern that reflects the appendages. (B) In 11 mm embryos, the crests of
a series of epidermal waves (see Fig. 1B) are densely innervated from below. The innervation of a single epidermal crest is viewed from the side,
showing the many nerve fascicles terminating at the skin surface. (C) The bottom epidermal wall of each appendage forms from caudal to rostral.
In 13 mm embryos, just prior to the growth of this lower layer of epidermis (see arrowhead, Fig. 1D), the deep portion of the innervating fascicles
begins to move rostrally (arrowhead). (D) In 15 mm and later embryos, the innervating nerve fascicles must make a complete
‘U
-turn’ to go around the deep layer of epidermis and reach their peripheral skin targets (see also Fig. 1E).
Fig. 3. Refinement of innervation patterns during the
course of development. (A1,2) In 11 mm stage embryos,
two different areas of the nose reveal the beginnings of
appendage-specific innervation patterns. In A1, an area
where the epidermal crests and troughs have formed
shows dense innervation of the crest and loss of
innervation from the trough (arrowhead) between the
precursors to appendages 2 and 3. In a more lateral area
(A2), where crests and troughs have not yet formed,
there is a uniform pattern of innervation. (B1,2) At a
later stage, the innervation of the crests is more refined
(B1). Higher magnification (B2) reveals the presence of
numerous filopodia and growth cones (arrowhead). The
adult pattern of punctate neurite distribution has not yet
emerged. (C1,2) In 20 mm embryos, the epidermal
cylinders of each appendage have formed, and the
internal walls are very densely innervated by many nerve
fascicles (C1). A punctate distribution of neurites has
formed in a pattern similar to the adult distribution (C2).
The clusters of nerve terminals reflect the future
distribution of epidermal sensory organs in the adult (see
Catania, 1995a,b and arrowheads in Fig. 6).
Development of the mole’s star nose 2723
Fig. 4. Postnatal development of the star. (A) In newborn moles, the appendages remain embedded in the epidermis of the face. (B) At
approximately 1 week, the appendages emerge from the side of the face as the surrounding epidermis sloughs. (C) Shortly thereafter the
appendages detach and bend forward into the adult pattern. As a result of this ‘backward’ formation, the rostralmost tissue of the adult nose is
derived from the caudalmost tissue of the embryonic nose (see Fig. 5C). Scale bars, 500 µm.
layer forms the bottom wall of each appendage, separating the
connective tissue of the dermis within each appendage from
the dermis and mesenchyme that form the center of the snout
(arrow, Fig. 1D). The deep epidermal layer grows from the
posterior snout towards the anterior snout, and the troughs of
the waves simultaneously extend slightly downward to meet
and fuse with the new layer of epidermis. At the same time,
the deep portions of the innervating nerve fibers move ahead
of the extending epidermis to maintain contact with their
targets (arrowheads, Fig. 2).
Towards the end of this process, in 20 mm embryos (just
prior to birth), there is a proliferation of epidermal cells that
seems to involve the entire rostral snout. As a result, each
primordial appendage forms a separate epidermal cylinder
within the hypertrophied epidermis (arrowheads, Fig. 1E) open
to the deep connective tissue only at the rostral end, near the
nares. The many nerve fascicles innervating an appendage
must pass through this small remaining opening, making a ‘Uturn’ to reach targets within the appendage (arrow, Fig. 2D).
Fig. 5. An adult mole and two ways that nasal appendages might
develop. (A) A star-nosed mole emerges from its tunnel, showing the
unusual star consisting of 22 fleshy appendages. The appendages are
densely innervated epidermis, have a rich blood supply and are
moved by tendons that connect to facial muscles. (B) A simplified
diagram of appendage formation through body-wall outgrowth.
Some variation of body-wall outgrowth is a basic stage in the
formation of nearly all animal appendages. This mechanism may be
conserved from a Precambrian ancestor of modern metazoans (see
text). (C) The unique developmental sequence for the nasal
appendages of the star. Rather than developing by outgrowth, they
begin as longitudinal cylinders embedded in the side of the face. The
cylinders of epidermis subsequently emerge and rotate forward, so
that the original embryonic orientation of the precursor tissue is
reversed. The colors denote the embryonic origins of the tissues that
make up the appendages in each of the two processes. During the
formation of the nasal appendages, caudal embryonic tissue of the
snout (red) detaches and becomes the most rostral tissue on the adult
nose. This is contrasted with the result of body wall outgrowth
(arrowheads).
With these processes complete, the basic outline of the
appendages is in place. Each now consists of a separate
cylindrical unit with a densely innervated epidermal wall
(Fig. 3C1). At this stage (20 mm), the nerve terminals that
contact the skin surface form a series of clusters in a periodic
pattern consistent with the distribution of sensory organs seen
later in the adult (arrowheads, Fig. 3C2).
In newborn moles (Fig. 4A), the appendages remain
embedded in the facial epidermis, giving an external
appearance that is surprisingly less adult-like than previous
embryonic stages. But the nasal appendages soon emerge from
2724 K. C. CATANIA, R. G. NORTHCUTT AND J. H. KAAS
Fig. 6. The adult nose of Townsend’s mole (Scapanus townsendi)
showing separate raised subdivisions of epidermis on the side of the
face. The star may have evolved from a similar ancestral condition
through progressive elevation of the raised epidermis, which contains
numerous sensitive touch organs called Eimer’s organs (small raised
domes, arrowheads). The same small receptor organs cover the
appendages of the star-nosed mole (Catania, 1995a,b). The receptors
in Scapanus townsendii are elevated relative to the nearby caudal
epidermis that does not contain sensory organs, which may allow for
increased tactile receptivity for the sensitive touch organs. Compare
the appearance of the nose of this adult mole with the early
embryonic stage in Fig. 1B.
the side of the face, presumably through programmed cell
death, as the once hypertrophied epidermis sloughs from
around the appendages (Fig. 4B). Roughly 1 week after birth,
the appendages break free from the side of the face and rotate
forward to form the adult star (Figs 4C, 5A).
To summarize this complex developmental sequence
(Fig. 5C), the nasal appendages form and emerge from the side
of the face and then rotate forward to form the adult pattern.
As a result of this ‘backwards’ formation, the rostral tissue of
the appendages is derived from caudal embryonic tissue of the
snout while the caudal tissue of the appendages is derived from
the rostral embryonic tissue of the snout. There is essentially
no outgrowth phase in this developmental sequence, and it
results in a reversal of the original embryonic orientation of the
tissue that forms the appendages. This developmental sequence
is manifestly different from the formation of other animal
appendages (Fig. 5B).
Discussion
The development and evolution of animal appendages have
been extensively studied in a number of species. In each case,
animal appendages originate as outgrowths of the body wall.
Well-known examples include the embryonic formation of
arthropod appendages and the tetrapod limb (for an account of
postnatal horn and antler development, see Goss, 1983). The
legs, antennae, mouthparts and wings of insects form from
imaginal disks that telescope outwards to produce each
respective structure (Gerhart and Kirschner, 1997b). In
Fig. 7. Two examples of common abnormalities of the star. (A) A
nose with an extra nasal appendage on the animal’s left side. Sudden
duplications such as this could provide the basis for progressive
elaboration from an ancestor with fewer appendages (see Fig. 6).
(B) A nose missing a nasal ray (although there is a partial duplication
of the tip of ray 6). We estimate that approximately 5–6 % of the
population has an abnormal nose. Clearly, there is relatively
widespread variation of the nasal anatomy upon which selection
might act, although we have not explored the genetic basis of these
variations.
tetrapods, a limb bud extends from the body wall to
successively produce differentiated cells in a proximal-todistal sequence of limb elements (Hinchliffe and Johnson,
1980). Later, the individual digits are initially sculpted by the
selective death (Hamburger and Hamilton, 1951) of
intervening cells in the handplate, and this is followed by
growth (Martin, 1990). Several stages of tetrapod digit
formation are shown alongside the nose formation in the mole
embryos (Fig. 1A–C) and their development can be contrasted
with nasal appendage development.
Tetrapod digits form by separation from a flattened
outgrowth or handplate and retain their original embryonic
orientation. In contrast, the nasal appendages of the star-nosed
mole unfold from the side of the face. This process requires
the growth of a new deep layer of epidermis to form both the
bottom wall of the appendages and the remaining side of the
face from which the appendages later emerge. It also requires
the rearrangement of innervating fibers (Fig. 2) and the rich
blood supply to the appendages (not shown), and results in the
previously described reversal of the orientation of precursor
tissues (Fig. 5C). What might account for such an unusual, and
seemingly inefficient, way of constructing the nasal
appendages?
A remarkable feature of appendage development is the
conservation of gene expression during morphogenesis in
different phyla. Homologous genes provide anterior–posterior
(hedgehog/Sonic hedgehog) and proximal–distal (fringe/
Radical fringe) patterning information in both insects and
tetrapods (Shubin et al., 1997). The Distal-less homeotic gene
Development of the mole’s star nose 2725
or its homologue are expressed during appendage formation in
diverse animal phyla, e.g. during the formation of echinoderm
tube feet, onychophoran lobopodia, tetrapod limbs, insect
appendages and sea urchin spines (Panganiban et al., 1997).
These studies (Panganiban et al., 1997; Raff, 1996; Shubin et
al., 1997) suggest that the genetic machinery for appendage
formation is phylogenetically ancient and may have helped
signal and regulate the formation of body-wall outgrowths in
a Precambrian ancestor.
In the star-nosed mole, however, the development of the
recently evolved nasal appendages suggests precursors of a
different form, such as sheets of sensory receptors or ‘protoappendages’ on the side of an ancestor’s snout, which became
progressively elevated over successive generations. Such a
recapitulatory argument (Dawkins, 1987; Gould, 1977;
Northcutt, 1990) is appealing, but would be more compelling
with fossil evidence or supporting comparative data. Although
no fossilized mole noses have been found, nearly all other
extant moles have sheets of the same complex sensory receptors
(Eimer’s organs) making up the epidermis of their snout in a
small, uniform epithelium around the unspecialized nares
(Catania, 1995b; Quilliam, 1966; Shibanai, 1988). But in one
North American species (Townsend’s mole Scapanus
townsendi), however, we discovered a set of ‘protoappendages’ extending caudally on the snout (Fig. 6). The
resemblance of the adult nose of this mole to the early
embryonic stages of the star-nosed mole (Fig. 1B) is striking.
This species might be called the Archaeopteryx of moles,
representing fairly well what would be expected of an
intermediate form between the least specialized moles and the
enigmatic star-nosed mole. Of course, this extant species is not
an ancestor of the star-nosed mole and, in fact, studies of mole
phylogeny suggest that its nose subdivisions evolved
independently of the appendages of the star-nosed mole
(Whidden, 1995; Yates and Moore, 1990). But Scapanus
townsendii does illustrate the tenability of such a hypothetical
ancestral species. Taken together with the developmental data,
it seems reasonable to propose that the star evolved through the
progressive elevation of strips of sensory receptors on the side
of the face, and that the stages of these ancestral ontogenies
have been conserved and built upon to produce the star. The
result is a novel developmental sequence that seems to
recapitulate many stages of ancestral anatomy (Gould, 1977).
Scapanus townsendi has only eight subdivisions on its face,
fewer than the 22 modules (11 per side) found on the star-nosed
mole. Once the basic developmental mechanism for appendage
production was in place, however, they might simply be
duplicated to produce the 22 appendages of the star. Such
meristic changes are a common occurrence in evolution (Raff,
1996) since duplication of somatic modules provides an
efficient means of adding to the body plan without the need to
reinvent the regulatory elements that produce each module. In
fact, duplications of nasal appendages are common in wild
populations of star-nosed moles (Fig. 7). We estimate that over
5 % of the population has an abnormal nose, consisting
of either extra or fewer nasal appendages (K. C. Catania,
unpublished data). This demonstrates that sufficient variability
exists upon which selection might act to increase (or decrease)
the number of nasal appendages. It also shows that there seems
to be a surprisingly high degree of variation in this presumably
critical structure, which contrasts with a much lower rate of
mutation in the tetrapod limb (Castilla et al., 1996; Zguricus et
al., 1998). Darwin (1859) made special note of such examples
in support of the Origin of Species, stating “in those cases in
which the modification has been comparatively recent and
extraordinarily great... we ought to find the generative
variability, as it might be called, still present in a high degree”.
The argument was that selection has had less time to ‘fix’ the
characteristics of recently evolved complex structures, which
are the recent product of selection for variations.
Flexibility or historical constraint?
At one level, these results demonstrate the flexibility of
evolutionary processes. While there seems to be a remarkable
conservancy in the basic mechanisms of appendage
development across metazoan phyla, there is also clearly the
potential for new developmental solutions to this ancient
morphogenetic problem. It has been stated that it is difficult to
think up anything very different from some actual product of
evolution (Maynard Smith, 1990). Here, we find a product of
evolution (the developmental sequence of the star) that we
might find hard even to imagine prior to this investigation. This
is perhaps because the developmental sequence of the nasal
appendages is not only unusual, but might also be considered
inefficient. To use an old example, it is difficult to envisage an
engineer proposing such a literally ‘backwards’ manner for
development of the nasal appendages.
Thus, at a different level of analysis, the development of the
nose seems to reflect the constraints imposed by biological
history (Gould, 1977, 1979, 1980). Perhaps there are more
efficient ways to produce the nasal appendages, such as the
outgrowth of the body wall seen for other metazoan
appendages, but evolution cannot plan ahead, it can only
‘tinker’ with the materials at hand (Jacob, 1977). The ontogeny
of the star provides a classic example of the outcome of such
tinkering. While different developmental stages may be altered
during the course of evolution (for a review, see Gould, 1977),
several early stages of the development of the nose of the mole
may be recalcitrant to change. For example, the crests of the
epidermal waves may produce the neurotrophic factors that
attract extending neurites to their appropriate appendagespecific targets. This possibility seems to be strengthened by
the presence of growth cones extending numerous filopodia
beneath the crests, up to at least 13 mm stage embryos
(Fig. B2). This ‘crest-and-trough’ stage may have existed in
the ancestor, which presumably had a snout similar to
Scapanus townsendi (Fig. 6). If this and other stages of the
development were critical during ancestral ontogenies, as
seems likely, then alteration of the nose may have occurred
primarily through modifications at the terminal end of ancestral
ontogenies, resulting in the apparent recapitulation of nasal
appendage evolution during development.
2726 K. C. CATANIA, R. G. NORTHCUTT AND J. H. KAAS
This work was supported by NIH grants MH58909 to
K.C.C. and NS 16446 to J.H.K.
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